Supporting information Table S1. Apatite modal abundance ...
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Supplementary Material (includes 3 tables numbered table S1 to S3)
Supplementary Material (includes 3 tables numbered table S1 to S3)
Table S1.
Collection of strains used in the study with their origins.
Strain ID
Source
JM221
Mathewson et al. 1987
17-2
Nataro et al. 1993
255/1-1
JP Girardeau-INRA
H10407
Evans et al. 1975
DAEC395
Forestier et al. 1996
DAECT2
Scaletsky et al. 2002
DAEC483
Forestier et al. 1996
DAEC7
Scaletsky et al. 2002
E2539-C1
Tornieporth et al. 1995
EDL1493
Tornieporth et al. 1995
ECOR10
Ochman and Selander 1984
ECOR20
Ochman and Selander 1984
ECOR13
Ochman and Selander 1984
ECOR1
Ochman and Selander 1984
DEC6a
Reid et al. 1999
ECOR24
Ochman and Selander 1984
ECOR17
Ochman and Selander 1984
ECOR4
Ochman and Selander 1984
EIEC85b
Escobar-Páramo et al. 2003
ECOR23
Ochman and Selander 1984
DAEC5
Scaletsky et al. 2002
DEC9a
Reid et al. 1999
DEC8b
Reid et al. 1999
55989
Bernier et al. 2002
248/1-2
JP Girardeau-INRA
DEC11a
Reid et al. 1999
DEC12a
Reid et al. 1999
DEC13a
Reid et al. 1999
ECOR68
Ochman and Selander 1984
H-19
Smith et al. 1983
DEC10a
Reid et al. 1999
469
Yves Germani-Inst.Pasteur
TX-1
Tornieporth et al. 1995
ECOR26
Ochman and Selander 1984
ECOR27
Ochman and Selander 1984
11097
Bernier et al. 2002
ECOR45
Ochman and Selander 1984
384P
Bernier et al. 2002
DAEC221
Forestier et al. 1996
DEC15a
Reid et al. 1999
DAECT437
Forestier et al. 1996
ECOR58
Ochman and Selander 1984
ECOR34
Ochman and Selander 1984
11074
Bernier et al. 2002
440
Yves Germani-Inst.Pasteur
DEC14a
Reid et al. 1999
DAEC126
Forestier et al. 1996
DAECT179
Forestier et al. 1996
ECOR70
Ochman and Selander 1984
DEC7a
Reid et al. 1999
SB01-97
Escobar-Páramo et al. 2003
SS92a
Escobar-Páramo et al. 2003
SB11-56
Escobar-Páramo et al. 2003
SD01-77
Escobar-Páramo et al. 2003
EDL933
Perna et al. 2001
RIMD0509952
Hayashi et al. 2001
ECOR37
Ochman and Selander 1984
EDL931
Bohm et al. 1992
DEC5d
Reid et al. 1999
DEC3a
Reid et al. 1999
DEC4a
Reid et al. 1999
DAEC218
Forestier et al. 1996
ECOR50
Ochman and Selander 1984
ECOR49
Ochman and Selander 1984
DAEC19
Scaletsky et al. 2002
56390
Bernier et al. 2002
DAECT192
Forestier et al. 1996
ECOR47
Ochman and Selander 1984
ECOR46
Ochman and Selander 1984
DAEC141
Forestier et al. 1996
DAEC162
Forestier et al. 1996
ECOR35
Ochman and Selander 1984
DAEC9
Scaletsky et al. 2002
ECOR40
Ochman and Selander 1984
ECOR41
Ochman and Selander 1984
DAECT14
Scaletsky et al. 2002
042
Nataro et al. 1985
DAECT19
Scaletsky et al. 2002
ECOR60
Ochman and Selander 1984
ECOR59
Ochman and Selander 1984
2348/69
Levine et al. 1978
DEC1a
Reid et al. 1999
DEC2a
Reid et al. 1999
ECOR51
Ochman and Selander 1984
ECOR52
Ochman and Selander 1984
CFT073
Welch et al. 2002
ECOR57
Ochman and Selander 1984
ECOR62
Ochman and Selander 1984
RS218
Silver et al. 1980
ECOR64
Ochman and Selander 1984
DAEC18
Scaletsky et al. 2002
EC7372
Pham et al. 1997
DAEC11
Scaletsky et al. 2002
IH11128
Vaisanen-Rhen 1984
DAEC20
Scaletsky et al. 2002
C1845
Bilge et al. 1989
381A
Bernier et al. 2002
DAEC213
Forestier et al. 1996
E. fergusonii
Lawrence et al. 1991
Literature cited
Bernier, C., P. Gounon, and C. Le Bouguénec. 2002. Identification of an aggregative adhesion fimbria (AAF) type III-encoding operon in enteroaggregative Escherichia coli as a sensitive probe for detecting the AAF-encoding operon family. Infect. Immun. 70:4302-4311.
Bilge, S. S., C. R. Clausen, W. LAu, and S. L. Moseley. 1989. Molecular characterization of a fimbrial adhesin, F1845, mediating diffuse adherence of diarrhea-associated Escherichia coli to HEp-2 cells. J. Bacteriol. 17:4281-4289.
Bohm, H., and H. Karch. 1992. DNA fingerprinting of Escherichia coli O157:H7 strains by pulsed-field gel electrophoresis. J. Clin. Microbiol. 30:2169-2172.
Escobar-Páramo, P., C. Giudicelli, C. Parsot, and E. Denamur. 2003. The evolutionary history of Shigella and enteroinvasive Escherichia coli revised. J. Mol. Evol. 57:140-148.
Evans, D. G., R. P. Silver, D. J. Evans, D. G. Chase, and S. L. Gorbach. 1975. Plasmid-controlled colonization factor associated with virulence in Escherichia coli enterotoxigenic for humans. Infect. Immun. 12:656-667.
Forestier, C., M. Meyer, S. Favre-Bonte, C. Rich, G. Malpuech, C. Le Bouguénec, J. Sirot, B. Joly, and C. De Champs. 1996. Enteroadherent Escherichia coli and diarrhea in children: a prospective case-control study. J. Clin. Microbiol. 34 :2897-2903.
Hayashi, T., K. Makino, M. Ohnishi, K. Kurokawa, K. Ishii, K. Yokoyama, C.-G. Han, E. Ohtsubo, K. Nakayama, T. Murata, M. Tanaka, T. Tobe, T. Iida, H. Takami, T. Honda, C. Sasakawa, N. Ogasawara, S. Yasunaga, T. Shiba, M. Hattori, and H. Shinagawa. 2001. Complete genome sequence of enterohemorragic Escherichia coli O157:H7 and genomic comparison with laboratory strain K-12. DNA Res. 8:11-22.
Lawrence, J. G., H. Ochman, and D. L. Hartl. 1991. Molecular and evolutionary relationships among enteric bacteria. J. Gen. Microbiol. 137:1911-1921.
Levine, M. M., E. J. Bergquist, D. R. Nalin, D. H. Waterman, R. B. Hornick, C. R. Young, S. Stoman, and B. Rowe. 1978. Escherichia coli strains that cause diarrhea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet I:119-122.
Mathewson, J. J., R. A. Oberhelman, H. L. Dupont, F. Javier de la Cabada , and E. V. Garibay. 1987. Enteroadherent Escherichia coli as a cause of diarrhea among children in Mexico. J Clin Microbiol. 25:1917-9.
Nataro, J. P., M. M. Baldini, J. B. Kaper, R. E. Black, N. Bravo, and M. M. Levine. 1985. Detection of an adherence factor of enteropathogenic Escherichia coli with DNA probe. J. Infect. Dis. 152:560-563.
Nataro, J. P., D. Yikang, J. A. Giron, S. J. Savarino, M. H. Kothary, and R. Hall. 1993. Aggregative adherence fimbria I expression in enteroaggregative Escherichia coli requires two unlinked plasmid regions. Infect. Immun. 6:1126-1131.
Ochman, H., and R. K. Selander. 1984. Standard reference strains of Escherichia coli from natural populations. J. Bacteriol. 157:690-692.
Perna, N. T., G. Plunkett III, V. Burland, B. Mau, J. D. Glasner, D. J. Rose, G. F. Mayhew, P. S. Evans, J. Gregor, H. A. Kirkpatrick, G. Posfais, J. Hacket, S. Klink, A. Boutin, Y. Shao, L. Miller, E. J. Grotbeck, N. W. Davis, A. Lim, E. T. Dimalanta, K. D. Potamousis, J. Apodaca, T. S. Anantharaman, J. Lin, G. Yen, D. C. Schwartz, R. A. Welch, and F. R. Blatner. 2001. Genome sequence of enterohemorrhagic Escherichia coli O157:H7. Nature 409:529-533.
Pham, T. Q., P. Goluszko, V. Popov, S. Nowicki, and B. J. Nowicki. 1997. Molecular cloning and characterization of Dr-II, a nonfimbrial adhesin-I-like adhesin isolated from gestational pyelonephritis-associated Escherichia coli that binds to decay-accelerating factor. Infect. Immun. 65:4309-4318.
Reid, S. D., C. J. Herbelin, A. C. Bumbaugh, R. K. Selander, and T. S. Whittam. 2000. Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406:64-67.
Scaletsky, I. C., S. H. Fabbricotti, R. L. Carvalho, C. R. Nunes, H. S. Maranhao, M. B. Morais, and U. Fagundes-Neto. 2002. Diffusely adherent Escherichia coli as a cause of acute diarrhea in young children in Northeast Brazil: a case-control study. J. Clin. Microbiol. 40:645-648.
Silver, R. P., W. Aaronson, A. Sutton, and R. Schneerson. 1980. Comparative analysis of plasmids and some metabolic characteristics of Escherichia coli K1 from diseased and healthy individuals. Infect. Immun. 29:200-206.
Smith, H. W., P. Green, and Z. Parsell. 1983. Vero cell toxins in Escherichia coli and related bacteris:transfer by phage and conjugation and toxic action in laboratory animals, chicken and pigs. J. Gen. Microbiol. 129:3121-3137.
Tornieporth, N. G., J. John, K. Salgado, P. de Jesus, E. Latham, M. C. Melo, S. T. Gunzburg, and L. W. Riley. 1995. Differentiation of pathogenic Escherichia coli strains in Brazilian children by PCR. J. Clin. Microbiol. 33:1371-1374.
Vaisanen-Rhen, V. 1984. Fimbria-like hemagglutinin of Escherichia coli O75 strains. Infect. Immun. 46:401-407.
Welch, R. A., V. Burland, G. Plunkett III, P. Redford, P. Roesch, D. Rasko, E. L. Buclkes, S.-R. Liou, A. Boutin, J. Hackett, D. Stroud, G. F. Mayhew, D. J. Rose, S. Zhou, D. C. Schwartz, N. T. Perna, H. L. T. Mobley, M. S. Donnenberg, and F. R. Blatner. 2002. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA 99:17020-17024.
Table S2
List of the primers used for the sequencing of the six essential genes (trpA to polB) used in the strain phylogenetic analysis as well as those used to generate the specific probes for detecting the presence of the different VFs and to perform their sequences.
Gene
Primer sequence
Source
trpA
5’-ATGGAACGCTACGAATCTCTGTTTGCCC-3’
Escobar-Páramo et al. 2003
5’-TCGCCGCTTTCATCGGTTGTACAAA-3’
trpB
5’-ACAATGACAACATTACTTAACCCCT-3’
Escobar-Páramo et al. 2003
5’-TTTCCCCTCGTGCTTTCAAAATATC-3’
pabB
5’-TTTTACACTCCGGCTATGCCGATCA-3’
Guttman and Dykhuizen 1994
5’-GCTGCGGTTCCAGTTCGTCGATAAT-3’
putP
5’-GCGACGATCCTTTACACCTTTATTG-3’
Escobar-Páramo et al. 2003
5’-CGCATCGGCCTCGGCAAAGCG-3’
icd
5’-GAAAGTAAAGTAGTTGTTCCGG-3’
Escobar-Páramo et al. in press
5’-GATGATCGCGTCACCAAAYTC-3’
polB
5’-TCAACGCCTGGTTTGCCAACTA-3’
Bjedov et al. 2003
5’-TCCAGTTCTAATGCGCTGGTCA-3’
papC
5’-GACGGCTGTACTGCAGGGTGTGGCG-3’
Le Bouguenec et al., 1992
5’-ATATCCTTTCTGCAGGGATGCAATA-3’
papG
5’-GGGATGAGCGGGCCTTTGAT-3’
Johnson and Brown 1996
5’-CGGGCCCCCAAGTAACTCG-3’
5’-GGCCTGCAATGGATTTACCTGG-3’
5’-CCACCAAATGACCATGCCAGAC-3’
sfa/foc
5’-CTCCGGAGAACTGGGTGCATCTTAC-3’
Le Bouguenec et al., 1992
5’-CGGAGGAGTAATTACAAACCTGGCA-3’
sfaS
5’-GTGGATACGACGATTACTGTG-3’
Johnson and Stell 2000
5’-CCGCCAGCATTCCCTGTATTC-3’
focG
5’-CAGCACAGGCAGTGGATACGA-3’
Johnson and Stell 2000
5’-GAATGTCGCCTGCCCATTGCT-3’
iroN
5’-AATCTTACCGGCAATAGCGC-3’
Bonacorsi et al. 2003
5’-GCTATAACGCACGGAGTTAC -3’
hlyCA
5’-AGGTTCTTGGGCATGTATCCT-3’
Bingen et al. 1998
5’-TTGCTTTGCAGACTGCAGTGT-3’
cnf1
5’-CAGTGACCGGATCTCCGTTAT-3’
Picard et al. 2001
5’-CGTGTAATTCTTCTGTACTTCC-3’
hra
5’-CAGAAAACAACCGGTATCAG-3‘
Bingen-Bidois et al. 2002
5’-ACCAAGCATGATGTCATGAC-3’
chuA
5’-GACGAACCAACGGTCAGGAT-3’
Clermont et al. 2000
5’-TGCCGCCAGTACCAAAGACA-3’
iucC
5'-AAACCTGGTTTACGCAACTGT-3'
Bingen et al. 1998
5’-ACCCGTCTGCAAATCATGGAT-3’
afaBC/daaC
5’-GCTGGGCAGCAAACTGATAACTCTC-3’
Le Bouguenec et al., 1992
5’-CATCAAGCTGTTTGTTCGTCCGCCG-3’
afaD
5’-GAAAGCGGTAAGCTGAAGGC-3’
This study
5’-CCGGTGAAATAAATACTCTC-3’
M030
5'-GATCAGCGCCACAATTAC-3'
Blanc-Potard et al. 2002
5'-CAGTGGAGTCTGCTGCTC-3'
AA
5’-CTGGCGAAAGACTGTATCAT-3’
Baudry et al. 1990
5’-CAATGTATAGAAATCCGCTGTT-3’
eaeA
5’-GCAAATTTAGGTGCGGGTCAGCGTT-3’
Germani et al. 1997
5’-GGCTCAATTTGCTGAGACCACGGTT-3’
bfpA
5’-CAATGGTGCTTGCGCTTGCT-3’
Tornieporth et al. 1995
5’-GCCGCTTTATCCAACCTGGT-3’
ST
5’-TCTGTATTGTCTTTTTCACC-3’
Tornieporth et al. 1995
5’-TTAATAGCACCCGGTACAAGC-3’
LT
5’-GCGACAAATTATACCGTGCT-3’
Tornieporth et al. 1995
5’-CCGAATTCTGTTATATATGT-3’
stx1
5’-GAAGAGTCCGTGGGATTACG-3’
Pollard et al. 1990
5’-AGCGATGCAGCTATTAATAA-3’
stx2
5’-TTAACCACACCCACGGCAGT-3’
Pollard et al. 1990
5’-GCTCTGGATGCATCTCTGGT-3’
ehxA
5’-ACGATGTGGTTTATTCTGGA-3’
Schmidt et al. 1995
5’-CTTCACGTCACCATACATAT-3’
ipaB
5’-GGACGCAATTCAGGATATCAAGGAG-3’
Escobar-Páramo et al. 2003
5’-GCCCCAAGTATTTTCCCAACACAAC-3’
Literature cited
Baudry, B., S. J. Savarino, P. Vial, J. B. Kaper, and M. M. Levine. 1990. A sensitive and specific DNA probe to identify enteroaggregative Escherichia coli, a recently discovered diarrheal pathogen. J. Infect. Dis. 161:1249-1251.
Bjedov, I., G. Lecointre, O. Tenaillon, C. Vaury, M. Radman, F. Taddei, E. Denamur, and I. Matic. 2003. Polymorphism of gene encoding SOS polymerases in natural populations of Escherichia coli. DNA Repair 2:417-426.
Bingen, E., B. Picard, N. Brahimi, S. Mathy, P. Desjardins, J. Elion, and E. Denamur. 1998. Phylogenetic analysis of Escherichia coli strains causing neonatal meningitis suggests horizontal gene transfer from a predominant pool of highly virulent B2 group strains. J. Infect. Dis. 177:642-650.
Bingen-Bidois, M., O. Clermont, S. Bonacorsi, M. Terki, N. Brahimi, C. Loukil, D. Barraud, and E. Bingen. 2002. Phylogenetic analysis and prevalence of urosepsis strains of Escherichia coli strains bearing pathogenicity islands-like domains. Infect. Immun. 70:3216-3226.
Blanc-Potard, A.-B., C. Tinsley, I. Scaletsky, C. Le Bouguenec, J. Guignot, A. L. Servin, X. Nassif, and M.-F. Bernet-Camard. 2002. Representational difference analysis between Afa/Dr diffusely adhering Escherichia coli and non-pathogenic E. coli K-12. Infect. Immun. 70:5503-5511.
Bonacorsi S., O. Clermont, V. Houdoin, C. Cordevant, N. Brahimi, A. Marecat, C. Tinsley, X. Nassif, M. Lange, and E. Bingen. 2003. Molecular analysis and experimental virulence of French and North American Escherichia coli neonatal meningitis isolates: identification of a new virulent clone. J. Infect. Dis. 187:1895-1906.
Clermont, O., S. Bonacorsi, and E. Bingen. 2000. Rapid and simple determination of the Escherichia coli phylogenetic groups. Appl. Environ. Microbiol. 66:4555-4558.
Escobar-Páramo, P., C. Giudicelli, C. Parsot, and E. Denamur. 2003. The evolutionary history of Shigella and enteroinvasive Escherichia coli revised. J. Mol. Evol. 57:140-148.
Escobar-Páramo, P., A. Sabbagh, P. Darlu, O. Pradillon, C. Vaury, G. Lecointre, and E. Denamur. Decreasing the effects of horizontal gene transfer on bacterial phylogeny: the Escherichia coli case study. Mol. Phylogenet. Evol. in press.
Germani, Y., E. Begaud, and C. Le Bouguenec. 1997. Detection of the Escherichia coli attaching and effacing gene (eaeA) as in enteropathogenic strains by polymerase chain reaction. Res. Microbiol. 148:177-181.
Guttman, D. S., and D.E. Dykhuizen. 1994. Detecting selective sweeps in naturally occurring Escherichia coli. Genetics 138:993-1003.
Johnson, J. R., and J. J. Brown. 1996. A novel multiply-primed polymerase chain reaction assay for identification of variant papG genes encoding the Gal (a1-4)Gal-binding PapG adhesins of Escherichia coli. J. Infect. Dis. 173:920-926.
Johnson, J. R., and A. L. Stell. 2000. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J. Infect. Dis. 181:261-272.
Le Bouguenec, C., M. Archambaud, and A. Labigne. 1992. Rapid and specific detection of the pap, afa, and sfa adhesin-encoding operons in uropathogenic Escherichia coli strains by polymerase chain reaction. J. Clin. Microbiol. 30:1189-1193.
Picard, B., P. Duriez, S. Gouriou, I. Matic, E. Denamur, and F. Taddei. 2001. Mutator natural Escherichia coli isolates have an unusual virulence phenotype. Infect. Immun. 69:9-14.
Pollard, D. R., W. M. Johnson, H. Lior, S. D. Tyler, and K. R. Rozee. 1990. Rapid and specific detection of verotoxin genes in Escherichia coli by polymerase chain reaction. J. Clin. Microbiol. 28:540-545.
Schmith, H., L. Beutin, and H. Karch. 1995. Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933. Infect. Immun. 63:1055-1061.
Tornieporth, N. G., J. John, K. Salgado, P. de Jesus, E. Latham, M. C. Melo, S. T. Gunzburg, and L. W. Riley. 1995. Differentiation of pathogenic Escherichia coli strains in Brazilian children by PCR. J. Clin. Microbiol. 33:1371-1374.
Table S3: Extraintestinal virulence genotypes of studied strains and their PAI-like content
Strains
Phylo group
sfa/focDE
Adhesin type
iroN
iucC
papC
papG
allele
hlyCA
cnf1
hra
PAI-like type*
17-2
A
-
-
+
+
II
+
-
-
PAI ICFT073
ECOR24
A
-
-
+
+
II
+
-
+
PAI ICFT073
DEC9a
A
-
-
-
-
-
+
-
+
248/1-2
B1
-
+
-
+
-
-
-
+
ECOR58
B1
+
foc
+
-
-
-
-
-
-
PAI III536
DAECT179
C
-
-
+
+
III
+
+
+
PAI IIJ96
DEC7a
C
-
-
-
-
-
+
-
-
ECOR50
D
-
-
+
+
II
-
-
+
ECOR49
D
-
-
+
+
II
-
-
-
ECOR46
D
-
-
-
+
III
-
-
+
DAEC162
D
-
-
-
+
-
-
-
-
ECOR40
D
-
-
+
+
II
-
-
-
ECOR41
D
-
-
+
+
II
-
-
-
ECOR60
B2
+
foc
+
-
+
III
+
+
+
PAI III536 + PAI IIJ96
ECOR51
B2
+
foc
+
+
+
III
+
+
+
PAI III536 + PAI IIJ96
ECOR52
B2
+
foc
+
-
+
III
+
+
+
PAI III536 + PAI IIJ96
CFT073
B2
+
foc
+
+
+
II
+
-
-
PAI III536 + PAI ICFT073
ECOR57
B2
+
foc
+
+
+
II
-
-
-
PAI III536
ECOR62
B2
-
+
+
+
II
-
-
-
RS218
B2
+
sfa
+
-
+
III
+
+
+
PAI III536 + PAI IIJ96
ECOR64
B2
+
foc
+
-
-
-
-
-
-
PAI III536
EC7372
B2
-
-
+
+
II
+
-
-
PAI ICFT073
* PAI-like types were defined by simultaneous identification of different characteristic virulence factors such as sfa/foc and iroN (PAI III536); papGII, hly and iucC (PAI ICFT073); and hly, cnf1 and hra with or without pap (PAI IIJ96) (Bonacorsi et al. 2003)
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